Climate Effects on Native Plants in Swiss Botanical Gardens Inauguraldissertation der Philosophisch-naturwissenschaftlichen Fakultät der Universität Bern vorgelegt von Christine Föhr von Eriswil (BE) Leiter der Arbeit: Prof. Dr. Markus Fischer Institut für Pflanzenwissenschaften, Botanischer Garten und Oeschger Zentrum, Universität Bern Climate Effects on Native Plants in Swiss Botanical Gardens Inauguraldissertation der Philosophisch-naturwissenschaftlichen Fakultät der Universität Bern vorgelegt von Christine Föhr von Eriswil (BE) Leiter der Arbeit: Prof. Dr. Markus Fischer Institut für Pflanzenwissenschaften, Botanischer Garten und Oeschger Zentrum, Universität Bern Von der Philosophisch-naturwissenschaftlichen Fakultät angenommen. Der Dekan: Bern, 21. September 2015 Prof. Dr. Gilberto Colangelo Public defense at the Institute of Plant Sciences (University of Bern) September 21, 2015 Promotion Committee Prof. Dr. Markus Fischer Institute of Plant Sciences, Botanical Garden and Oeschger Center University of Bern Prof. Dr. Jasmin Joshi University of Potsdam Chairman Prof. Dr. Willy Tinner Institute of Plant Sciences University of Bern Table of contents Chapter 1 General introduction………………………………………………...….…….1 Chapter 2 Warmer climate than in their natural range reduces the performance of 165 native plant species across 10 botanical gardens in Switzerland…………………………………….11 Chapter 3 Phenological shifts and flower visitation of 185 lowland and alpine species growing in a lowland botanical garden…………………………………………………………………...………….39 Chapter 4 Adaptive responses to cultivation and to novel environmental conditions in rare and common alpine plant species grown in botanical gardens…………..……..……..71 Chapter 5 Summary and conclusions…………….…………………………............99 References……………………………………………………….…………………………….....107 Danksagung…………………………………………………………..………...………………..118 Erklärung…………………………………………………………..…………..……………...….120 Curriculum vitae………………………………………………….…………..……………….121 Chapter 1 General introduction The impact of climate change on plant performance Recent anthropogenic climate change has led to a mean global temperature increase of 0.74°C in the last century (IPCC 2007). Similar trends have been observed in Switzerland, with a mean temperature increase of 1.2°C/100 years, a decrease in number of frost days, an elevational rise of the zero degree level, and increase of precipitation in winter (Klimareport Meteoschweiz 2014). Abiotic factors such as temperature and precipitation directly influence vital physiological processes such as photosynthesis, respiration and growth in plants (Hughes 2000, Gurevitch et al. 2006). As every plant is physiologically adapted to the environment in which it is growing, changing climatic conditions may affect plant survival and reproduction. As a consequence, increasing mortality rates and decreasing reproductive rates within the populations may compromise the persistence of plant populations in the long-term. The change in abundance or the complete disappearance of a particular species in a habitat will have an impact on the community composition as other species will take over the available space (Hughes 2000, Lenoir et al. 2010, Gornish & Tylianakis 2013) and species interactions may become disrupted or altered (Parmesan 2006). Changes in the presence or abundance of species and altered species interactions may have an impact on the ecosystem as species traits directly influence ecosystem properties (Chapin et al. 2000, Hooper et al. 2005). Thus, by influencing the performance of plants, changing climatic conditions may ultimately lead to major changes at the community and ecosystem levels. Understanding the effects of climate change on plant performance is therefore essential to anticipate potential 1 Chapter 1 negative effects on species, communities and ecosystems and will help to set conservation priorities. Modeling studies predict that under ongoing climate change some species will no longer be able to grow at their present locations because of temperature or drought stress or changed interactions (e.g. competitive exclusion) with other species (Thomas et al. 2004, Ibáñez et al. 2006). As a result, many species are shifting their distribution range in latitude or elevation as they move together with the climate to which they are adapted (Grabherr et al. 1994, Sturm et al. 2001, Walther et al 2002, Parmesan & Yohe 2003, Stöckli et al. 2011, Pauli et al. 2012). However, species might be hindered in their movement by natural obstacles such as mountain ranges or large waters and by habitat fragmentation (Higgins et al. 2003, Meier et al. 2012). Furthermore, sessile organisms such as plant species might not be able to move fast enough due to dispersal limitation (Midgley et al. 2006, Engler et al. 2009). Thus, the movement ability of many plant species is unlikely to keep up with the expected fast climate change (Corlett & Westcott 2013, Cunze et al. 2013). For dispersal limited species, persistence under novel climatic conditions by adjusting their phenotype to the changing conditions (phenotypic plasticity) or by rapid genetic evolution (adaptation) is essential (Thuiller et al. 2008, Chevin et al. 2010). Transplantation and warming experiments have shown varying responses of plant performance to higher temperatures. For example, plant growth mainly increased under warmer conditions but sometimes also decreased (Arft et al. 1999, de Valpine & Harte 2001, Peñuelas et al. 2004, Trtikova et al. 2010, De Frenne et al. 2011). Studies that investigated the effect of increasing temperature on plant survival and reproduction reported a higher mortality (Angert & Schemske 2005) and higher as well as lower reproductive success (Arft et al. 1999, De Frenne et al. 2011). 2 General introduction However, most of the studies focused on one or few species which limits their strength and the generality of their conclusions. In addition, although positive responses in growth and reproduction have been detected, the long- term costs for these changes are largely unknown (Corlett & Westcott 2013). Moreover, if the magnitude of climate change exceeds the species’ tolerance or their ability for rapid evolutionary response, negative consequences for plant performance and population persistence are likely to occur, and species extinction risk will increase (Jump & Peñuelas 2005). Climatic conditions, particularly temperature, can strongly influence the timing of important plant life-history events, such as flowering time (Forrest & Miller-Rushing 2010). It has been shown that many plant species respond to global warming by flowering earlier in the season (Fitter & Fitter 2002, Menzel et al. 2006, Gordo & Sanz 2010, Ibáñez et al. 2010). Flowering earlier in the year can negatively affect the reproductive success of the plants (Burgess et al. 2007, Scheepens & Stöcklin 2013) due to an increased risk of flower bud damages by late frost events (Inouye 2008) and possible temporal mismatches in plant-pollinator interactions (Memmott et al. 2007, Hegland 2009, Kudo & Ida 2013, Petanidou et al. 2014). Such temporal mismatches in plant-pollinator interactions may occur as species vary in their temporal sensitivity and therefore respond differently to environmental cues (Parmesan & Yohe 2003, Forrest 2015). Mismatches in plant-pollinator interactions may contribute to an overall degradation of the interaction network within the community, if novel plant-pollinator interactions cannot be formed (Memmott et al. 2007, Kaiser-Bunbury et al. 2010, Burkle et al. 2013, Revilla et al. 2015). This may have substantial negative consequences on the persistence of both the plant and the pollinator populations. 3 Chapter 1 Rare and threatened plant species may be particularly susceptible to climate change (Maschinski et al. 2006; Marrero-Gómez 2007; Lawson 2010). They often occur in small and isolated populations of low genetic diversity which may be caused by genetic drift and inbreeding (Karron 1997). Low genetic diversity might negatively affect viability (Oostermeijer et al. 2003, Leimu et al. 2006) and through the loss of potentially adaptive alleles also the adaptive potential of the plant populations (Husband & Campbell 2004, Willi et al. 2006, Leimu and Fischer 2008, Jump et al. 2009). Additionally, species with restricted ranges often have a low dispersal ability (Gaston 1994). Weak dispersal would limit the plants’ ability to colonize new ecologically suitable habitats and shift their range with the climate they are adapted to. Rare plant species might also have more specialized plant- pollinator-interactions to increase the probability that removed pollen is deposited on the stigma of a conspecific plant (Orians 1997, Sargent & Otto 2006). However, specialized plant-pollinator interactions may render them particularly vulnerable in case of phenological mismatches and impede successful reproduction. Thus, due to the combination of multiple factors, especially rare and threatened plant species may face an increased extinction risk in future if effective conservation measures are not taken in time (Gurevitch et al. 2006). Consequences of ex-situ conservation for adaptation Species extinction risk is predicted to increase substantially in the next decades as a result of climate change (Thomas et al. 2004, Thuiller et al. 2005a). To prevent the potential loss of thousands of plant species, plant conservation needs to be an urgent priority (Wyse Jackson & Kennedy 2009). Plant conservation in the natural environment (in situ) alone